Only a subset of phosphoantigen-responsive γ9δ 2 T cells mediate protective tuberculosis immunity

Journal of Immunology

Volumn 181, Issue 7, 2008, Pages 4471-4484

  Spencer, Charles T ^a   Abate, Getahun ^a   Blazevic, Azra ^a   Hoft, Daniel F ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; T LYMPHOCYTE RECEPTOR DELTA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN; TOLL LIKE RECEPTOR; BACTERIAL ANTIGEN; HEMITERPENE; ISOPENTENYL DIPHOSPHATE; LYMPHOCYTE ANTIGEN RECEPTOR; ORGANOPHOSPHORUS COMPOUND;

ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL IMMUNITY; BACTERIAL INFECTION; CELL EXPANSION; CONTROLLED STUDY; DENDRITIC CELL; HUMAN; IMMUNOSTIMULATION; INFECTION PREVENTION; MICROBIAL ACTIVITY; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; SUPPRESSOR CELL; T LYMPHOCYTE SUBPOPULATION; AMINO ACID SEQUENCE; BIOSYNTHESIS; CELL CLONE; CELL LINE; COMPARATIVE STUDY; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INNATE IMMUNITY; LUNG TUBERCULOSIS; LYMPHOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; ANTIGENS, BACTERIAL; CELL LINE; CLONE CELLS; HEMITERPENES; HUMANS; IMMUNITY, INNATE; LYMPHOCYTE ACTIVATION; MOLECULAR SEQUENCE DATA; MYCOBACTERIUM BOVIS; ORGANOPHOSPHORUS COMPOUNDS; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTE SUBSETS; TUBERCULOSIS, PULMONARY;

EID: 58149311505     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.7.4471     Document Type: Article

References (49)

1. Worku, S., G. J. Gorse, R. B. Belshe, and D. F. Hoft. 2001. Canarypox vaccines induce antigen specific human γδ T cells capable of IFN-γ production. J. Infect. Dis. 184: 525-532. (Pubitemid 32783541)
2. Hoft, D. F., R. Brown, and S. Roodman. 1998. Bacille Calmette- Guérin vaccination enhances human γδ T cell responsiveness to mycobacteria suggestive of a memory-like phenotype. J. Immunol. 161: 1045-1054.
3. + T cells during mycobacterial infections. Science 295: 2255-2258.
4. Janis, E. M., S. H. E. Kaufmann, R. H. Schwartz, and D. M. Pardoll. 1989. Activation of γδ T cells in the primary immune response to Mycobacterium tuberculosis. Science 244: 713-716.
5. Alito, A., J. McNair, R. M. Girvin, M. Zumarraga, F. Bigi, J. M. Pollock, and A. Cataldi. 2003. Identification of Mycobacterium bovis antigens by analysis of bovine T-cell responses after infection with a virulent strain. Braz. J. Med. Biol. Res. 36: 1523-1531. (Pubitemid 37408042)
6. Jouen-Beades, F., E. Paris, C. Dieulois, J. F. Lemeland, V. Barre-Dezelus, S. Marret, G. Humbert, J. Leroy, and F. Tron. 1997. In vivo and in vitro activation and expansion of γδ T cells during Listeria monocytogenes infection in humans. Infect. Immun. 65: 4267-4272. (Pubitemid 27422087)
7. Ho, M., P. Tongtawe, J. Kriangkum, T. Wimonwattrawatee, K. Pattanapanyasat, L. Bryant, J. Shafiq, P. Suntharsamai, S. Looareesuwan, H. K. Webster, and J. F. Elliott. 1994. Polyclonal expansion of peripheral γ δ T cells in human Plasmodium falciparum malaria. Infect. Immun. 62: 855-862. (Pubitemid 24065565)
8. Verjans, G. M., R. W. Roest, K. A. van der, G. van Dijk, W. I. van der Meijden, and A. M. Osterhaus. 2004. Isopentenyl pyrophosphate-reactive Vγ9Vδ2 T helper 1-like cells are the major γδ T cell subset recovered from lesions of patients with genital herpes. J. Infect. Dis. 190: 489-493.
9. Li, B., M. D. Rossman, T. Imir, A. F. Oner-Eyuboglu, C. W. Lee, R. Biancaniello, and S. R. Carding. 1996. Disease-specific changes in γδ T cell repertoire and function in patients with pulmonary tuberculosis. J. Immunol. 157: 4222-4229. (Pubitemid 126449337)
10. Li, B., H. Bassiri, M. D. Rossman, P. Kramer, A. F. Eyuboglu, M. Torres, E. Sada, T. Imir, and S. R. Carding. 1998. Involvement of the fas/fas ligand pathway in activation-induced cell death of mycobacteria-reactive human γδ T cells: a mechanism for the loss of γδ T cells in patients with pulmonary tuberculosis. J. Immunol. 161: 1558-1567. (Pubitemid 28380590)
11. + T-cell responses during active mycobacterial coinfection of simian immunodeficiency virus SIV-mac-infected monkeys. J. Virol. 77: 2998-3006.
12. Eberl, M., M. Hintz, A. Reichenberg, A. K. Kollas, J. Wiesner, and H. Jomaa. 2003. Microbial isoprenoid biosynthesis and human γδ T cell activation. FEBS Lett. 544: 4-10. (Pubitemid 36628027)
13. Wesch, D., S. Marx, and D. Kabelitz. 1997. Comparative analysis of αβ and γ/δ T cell activation by Mycobacterium tuberculosis and isopentenyl pyrophosphate. Eur. J. Immunol. 27: 952-956. (Pubitemid 27155331)
14. Tanaka, Y., C. T. Morita, Y. Y. Tanaka, E. Nieves, M. B. Brenner, and B. R. Bloom. 1995. Natural and synthetic nonpeptide antigens recognized by human γδ T cells. Nature 375: 155-158.
15. Hintz, M., A. Reichenberg, B. Altincicek, U. Bahr, R. M. Gschwind, A. K. Kollas, E. Beck, J. Wiesner, M. Eberl, and H. Jomaa. 2001. Identification of (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate as a major activator for human γδ T cells in Escherichia coli. FEBS Lett. 509: 317-322. (Pubitemid 34015963)
16. Espinosa, E., C. Belmant, F. Pont, B. Luciani, R. Poupot, F. Romagne, H. Brailly, M. Bonneville, and J. J. Fournie. 2001. Chemical synthesis and biological activity of bromohydrin pyrophosphate, a potent stimulator of human γ δ T cells. J. Biol. Chem. 276: 18337-18344. (Pubitemid 37411407)
17. Gougeon, M. L., M. Malkovsky, R. Casetti, C. Agrati, and F. Poccia. 2002. Innate T cell immunity to HIV-infection: immunotherapy with phosphocarbohydrates, a novel strategy of immune intervention? Vaccine 20: 1938-1941.
18. Sicard, H., S. Ingoure, B. Luciani, C. Serraz, J. J. Fournie, M. Bonneville, J. Tiollier, and F. Romagne. 2005. In vivo immunomanipulation of Vγ9Vδ2 T cells with a synthetic phosphoantigen in a preclinical nonhuman primate model. J. Immunol. 175: 5471-5480. (Pubitemid 41456434)
19. Cendron, D., S. Ingoure, A. Martino, R. Casetti, F. Horand, F. Romagne, H. Sicard, J. J. Fournie, and F. Poccia. 2007. A tuberculosis vaccine based on phosphoantigens and fusion proteins induces distinct γδ and αβ T cell responses in primates. Eur. J. Immunol. 37: 549-565. (Pubitemid 46915593)
20. Worku, S., and D. F. Hoft. 2003. Differential effects of control and antigen-specific T cells on intracellular mycobacterial growth. Infect. Immun. 71: 1763-1773. (Pubitemid 36368705)
21. Worku, S., and D. F. Hoft. 2000. In vitro measurement of protective mycobacterial immunity: antigen specific expansion of T cells capable of inhibiting intracellular growth of BCG. Clin. Infect. Dis. 30: S257-S261. (Pubitemid 32250417)
22. Thurner, B., C. Roder, D. Dieckmann, M. Heuer, M. Kruse, A. Glaser, P. Keikavoussi, E. Kampgen, A. Bender, and G. Schuler. 1999. Generation of large numbers of fully mature and stable dendritic cells from leukapheresis products for clinical application. J. Immunol. Methods 223: 1-15. (Pubitemid 29096234)
23. Olive, C., P. A. Gatenby, and S. W. Serjeantson. 1992. Variable gene usage of T cell receptor γ- and δ-chain transcripts expressed in synovia and peripheral blood of patients with rheumatoid arthritis. Clin. Exp. Immunol. 87: 172-177.
24. Holtmeier, W., A. Hennemann, E. May, R. Duchmann, and W. F. Caspary. 2002. T cell receptor δ repertoire in inflamed and noninflamed colon of patients with IBD analyzed by CDR3 spectratyping. Am. J. Physiol. 282: G1024-G1034. (Pubitemid 34651609)
25. Rock, E. P., P. R. Sibbald, M. M. Davis, and Y. H. Chien. 1994. CDR3 length in antigen-specific immune receptors. J. Exp. Med. 179: 323-328.
26. Hanekom, W. A., J. Hughes, M. Mavinkurve, M. Mendillo, M. Watkins, H. Gamieldien, S. J. Gelderbloem, M. Sidibana, N. Mansoor, V. Davids, et al. 2004. Novel application of a whole blood intracellular cytokine detection assay to quantitate specific T-cell frequency in field studies. J. Immunol. Methods 291: 185-195.
27. Fisch, P., K. Oettel, N. Fudim, J. E. Surfus, M. Malkovsky, and P. M. Sondel. 1992. MHC-unrestricted cytotoxic and proliferative responses of two distinct human γ/δ T cell subsets to Daudi cells. J. Immunol. 148: 2315-2323.
28. Halary, F., M. A. Peyrat, E. Champagne, M. Lopez-Botet, A. Moretta, L. Moretta, H. Vie, J. J. Fournie, and M. Bonneville. 1997. Control of self-reactive cytotoxic T lymphocytes expressing γ δ T cell receptors by natural killer inhibitory receptors. Eur. J. Immunol. 27: 2812-2821. (Pubitemid 27478348)
29. Schwender, J., M. Seemann, H. K. Lichtenthaler, and M. Rohmer. 1996. Biosynthesis of isoprenoids (carotenoids, sterols, prenyl side-chains of chlorophylls and plastoquinone) via a novel pyruvate/glyceraldehyde 3-phosphate non-mevalonate pathway in the green alga Scenedesmus obliquus. Biochem. J. 316: 73-80. (Pubitemid 126732839)
30. Deetz, C. O., A. M. Hebbeler, N. A. Propp, C. Cairo, I. Tikhonov, and C. D. Pauza. 2006. γ Interferon secretion by human Vγ2Vδ2 T cells after stimulation with antibody against the T-cell receptor plus the Toll-Like receptor 2 agonist Pam3Cys. Infect. Immun. 74: 4505-4511.
31. Mokuno, Y., T. Matsuguchi, M. Takano, H. Nishimura, J. Washizu, T. Ogawa, O. Takeuchi, S. Akira, Y. Nimura, and Y. Yoshikai. 2000. Expression of Toll-like receptor 2 on γ δ T cells bearing invariant Vγ6/Vδ1 induced by Escherichia coli infection in mice. J. Immunol. 165: 931-940. (Pubitemid 30484761)
32. Means, T. K., S. Wang, E. Lien, A. Yoshimura, D. T. Golenbock, and M. J. Fenton. 1999. Human toll-like receptors mediate cellular activation by Mycobacterium tuberculosis. J. Immunol. 163: 3920-3927.
33. Chang, J. S., J. F. Huggett, K. Dheda, L. U. Kim, A. Zumla, and G. A. Rook. 2006. Myobacterium tuberculosis induces selective up-regulation of TLRs in the mononuclear leukocytes of patients with active pulmonary tuberculosis. J. Immunol. 176: 3010-3018.
34. von Meyenn, F., M. Schaefer, H. Weighardt, S. Bauer, C. J. Kirschning, H. Wagner, and T. Sparwasser. 2006. Toll-like receptor 9 contributes to recognition of Mycobacterium bovis Bacillus Calmette-Guerin by Flt3-ligand generated dendritic cells. Immunobiology 211: 557-565. (Pubitemid 44241634)
35. Wesch, D., S. Beetz, H. H. Oberg, M. Marget, K. Krengel, and D. Kabelitz. 2006. Direct costimulatory effect of TLR3 ligand poly(I:C) on human γ δ T lymphocytes. J. Immunol. 176: 1348-1354. (Pubitemid 43134276)
36. Morita, C. T., H. K. Lee, H. Wang, H. Li, R. A. Mariuzza, and Y. Tanaka. 2001. Structural features of nonpeptide prenyl pyrophosphates that determine their antigenicity for human γδ T cells. J. Immunol. 167: 36-41.
37. Evans, P. S., P. J. Enders, C. Yin, T. J. Ruckwardt, M. Malkovsky, and C. D. Pauza. 2001. In vitro stimulation with a non-peptidic alkylphosphate expands cells expressing Vγ2-Jγ1.2/Vδ2 T-cell receptors. Immunology 104: 19-27. (Pubitemid 32955390)
38. Miyagawa, F., Y. Tanaka, S. Yamashita, B. Mikami, K. Danno, M. Uehara, and N. Minato. 2001. Essential contribution of germline-encoded lysine residues in Jγ1.2 segment to the recognition of nonpeptide antigens by human γδ T cells. J. Immunol. 167: 6773-6779. (Pubitemid 33144167)
39. Martino, A., R. Casetti, A. Sacchi, and F. Poccia. 2007. Central memory Vγ9Vδ2 T lymphocytes primed and expanded by bacillus Calmette-Guerin-infected dendritic cells kill mycobacterial-infected monocytes. J. Immunol. 179: 3057-3064.
40. Poccia, F., B. Cipriani, S. Vendetti, V. Colizzi, Y. Poquet, L. Battistini, J. J. Fournié, and M. L. Gougeon. 1997. CD94/NKG2 inhibitory receptor complex modulates both anti-viral and anti-tumoral responses of polyclonal phosphoantigen-reactive Vγ9Vδ2 T lymphocytes. J. Immunol. 159: 6009-6017. (Pubitemid 127471537)
41. Vankayalapati, R., B. Wizel, S. E. Weis, H. Safi, D. L. Lakey, O. Mandelboim, B. Samten, A. Porgador, and P. F. Barnes. 2002. The NKp46 receptor contributes to NK cell lysis of mononuclear phagocytes infected with an intracellular bacterium. J. Immunol. 168: 3451-3457. (Pubitemid 34250410)
42. Lilienfeld-Toal, M., J. Nattermann, G. Feldmann, E. Sievers, S. Frank, J. Strehl, and I. G. Schmidt-Wolf. 2006. Activated γδ T cells express the natural cytotoxicity receptor natural killer p 44 and show cytotoxic activity against myeloma cells. Clin. Exp. Immunol. 144: 528-533.
43. Esin, S., G. Batoni, C. Counoupas, A. Stringaro, F. L. Brancatisano, M. Colone, G. Maisetta, W. Florio, G. Arancia, and M. Campa. 2008. Direct binding of human NK cell natural cytotoxicity receptor NKp44 to the surfaces of mycobacteria and other bacteria. Infect. Immun. 76: 1719-1727. (Pubitemid 351562017)
44. Brandes, M., K. Willimann, and B. Moser. 2005. Professional antigen-presentation function by human γδ T cells. Science 309: 264-268. (Pubitemid 40967855)
45. Allison, T. J., C. C. Winter, J. J. Fournie, M. Bonneville, and D. N. Garboczi. 2001. Structure of a human γδ T-cell antigen receptor. Nature 411: 820-824. (Pubitemid 32588108)
46. Bukowski, J. F., C. T. Morita, H. Band, and M. B. Brenner. 1998. Crucial role of TCR γ chain junctional region in prenyl pyrophosphate antigen recognition by γδ T cells. J. Immunol. 161: 286-293.
47. Lovitch, S. B., and E. R. Unanue. 2005. Conformational isomers of a peptide-class II major histocompatibility complex. Immunol. Rev. 207: 293-313. (Pubitemid 41415025)
48. Casetti, R., G. Perretta, A. Taglioni, M. Mattei, V. Colizzi, F. Dieli, G. D'Offizi, M. Malkovsky, and F. Poccia. 2005. Drug-induced expansion and differentiation of Vγ9Vδ2 T cells in vivo: the role of exogenous IL-2. J. Immunol. 175: 1593-1598. (Pubitemid 41023061)
49. Martino, A., R. Casetti, and F. Poccia. 2007. Enhancement of BCG-induced Th1 immune response through Vγ9Vδ2 T cell activation with non-peptidic drugs. Vaccine 25: 1023-1029. (Pubitemid 44937450)